The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples

Previously it has been shown that the hippocampus and neocortex can spontaneously reactivate ensemble activity patterns during
post-behavioral sleep and rest periods. Here we examined whether such reactivation also occurs in a subcortical structure, the ventral
striatum, which receives a direct input from the hippocampal formation and has been implicated in guidance of consummatory and
conditioned behaviors. During a reward-searching task on a T-maze, flanked by sleep and rest periods, parallel recordings were made
from ventral striatal ensembles while EEG signals were derived from the hippocampus. Statistical measures indicated a significant
amount of reactivation in the ventral striatum. In line with hippocampal data, reactivation was especially prominent during postbehavioral
slow-wave sleep, but unlike the hippocampus, no decay in pattern recurrence was visible in the ventral striatum across the first
40 min of post-behavioral rest. We next studied the relationship between ensemble firing patterns in ventral striatum and hippocampal
ripples?sharp waves, which have been implicated in pattern replay. Firing rates were significantly modulated in close temporal association
with hippocampal ripples in 25% of the units, showing a marked transient enhancement in the average response profile. Strikingly,
ripple-modulated neurons in ventral striatum showed a clear reactivation, whereas nonmodulated cells did not. These data suggest, first,
the occurrence of pattern replay in a subcortical structure implied in the processing and prediction of reward and, second, a functional
linkage between ventral striatal reactivation and a specific type of high-frequency population activity associated with hippocampal
replay.
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